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Brazilian free-tailed bats, like these in Texas, use song to court mates and defend territory.

When the bat sings The trills and chirps of bats can be as complex and meaningful as bird song—and may be a closer analog for human speech

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rchaeologists aren’t sure how the Governor’s Palace, a creamand-white limestone structure at Uxmal, Mexico, figured in Maya religious ceremonies. Its walls of carefully chiseled blocks are now crumbling; the chants of priests no longer echo in its halls. Yet if you’re quiet and observant, you’ll hear the songs of the current residents of the palace: bats. “Do you hear them?” asks Kirsten Bohn, a behavioral ecologist and bat expert at Florida International University in Miami. “It’s like the walls are singing.” It takes a moment to tune my ear to the right pitch, but once I do, I realize the air is filled with the bats’ soft, birdlike twitters, chirps, and trills. And this is not during the 1334

deep of the night, but in the middle of the day. So if you know where to look, you can see the bats, too. “Well, hello there, boo-boo,” Bohn says, peering into a long, narrow fissure that time and erosion have opened up between the wall’s stones. She presses her face close to the crack, squinting to get a better look at the mouse-sized bats sandwiched inside. I do the same, and once my eyes adjust to the dark of the crevice, I’m eye to eye with a brown-eyed Nyctinomops laticaudatus, the broad-eared bat. He scuttles back into his rocky lair, but I can still see his chattering jaws: “Zzzzzzzzz.” “That’s an aggressive warning call,” Bohn explains. “He’s telling us to back off. He doesn’t want to bother with us; he wants to do what’s important—[which is] to sing.”

Bohn has traveled to Uxmal to capture the songs of this and dozens of other broadeared bats scrunched inside the ruin’s walls in order to study the evolution and function of bat song. Biologists commonly use the word “song” to describe any acoustic displays by males, including the simple calls of frogs, insects, and many other creatures. Bohn, however, reserves “song” for something as complex as bird song—calls “composed of multiple syllables combined in a specific way, and which have repeatable patterns and rhythm.” By this reckoning, many birds, some cetaceans, and humans sing. So, it turns out, do some bats. That bats emit any kind of song comes as a surprise to most people, partly because we tend to think chiefly of their echolocation calls, ultrasonic sounds beyond sciencemag.org SCIENCE

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PHOTO: © MERLIN D. TUTTLE, BAT CONSERVATION INTERNATIONAL, WWW.BATCON.ORG

By Virginia Morell

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PHOTOS: (TOP TO BOTTOM) JENS RYDELL; KIRSTEN BOHN; GRACE SMARSH/TEXAS A&M UNIVERSITY

our hearing, or their short, sharp social calls. It’s also a surprise because it is so rare for a mammal to sing like a songbird. “So why do bats?” Bohn asks. “What are the social and environmental pressures that have led them to evolve this ability, which is so mentally demanding?” To find out, researchers are seeking out bat troubadours from New Zealand to Africa. Already, studies by Bohn, her collaborator Michael Smotherman, a neurophysiologist at Texas A&M University, College Station, and others have shown that like many songbirds, most bat songsters are male, live in polygynous societies where males mate with more than one female, and tend to sing during the mating season to court females and defend territories. Their complex songs are probably not innate, and so require vocal learning, as bird song and human speech do. At least one species of bat appears to have a specialized neural loop in its forebrain, analogous to the circuit in songbirds that underlies vocal learning. Geneticists have added another parallel: The FOXP2 gene, which is tied to vocal learning in humans and birds, has also been under intense selection in bats. “There’s much left to discover,” says Mirjam Knörnschild, a behavioral ecologist and bat song expert at the University of Ulm in Germany. But already, the bat song enthusiasts are wondering if these winged mammals can help explain the evolution of complex vocal abilities overall— including that of their fellow mammals, human speech.

To study the details of bat song, Smotherman and others have started captive colonies—captive bats won’t sing alone, underscoring the social nature of bat song. But researchers also venture to caves, trees, parking garages, and ruins, studying known songster species and searching for new ones. “You have to know which ones sing and which ones don’t to fully understand song in bats,” Bradbury says. Answering that question is one reason why Bohn traveled to Uxmal. “Do all the Molossidae species—there are at least 100—and their related genera sing?” she asks. “If they don’t, why not? I’m trying to figure out how and why this complex form of communication came about.” In spite of our presence, the broadeared bats are still twittering to each other. Close to the wall, I catch a whiff of a strong, pungent odor. “They sure smell like males,” Bohn says, taking another peek at the bats. “Yuck. It’s got to be a bachelors’ pad.” In the related Brazilian free-tailed bat that Bohn studies back home in the United States, each male stakes out a territory within the larger mixed roost and sings both to lure females in for mating and to keep other males out. The broad-eared bat may have similar arrangements, but no one knows; Bohn is only now exploring its habits. “They’re peeing on everything, marking every bit of their territories,” she observes. “And just singing their hearts out.” So far, scientists have found few similarities in the notes or syllables used by the various species of bats, or in the structure of their tunes. But SCIENTISTS HAVE KNOWN that in three major papers, one published bats sing since at least 1974, when just last year in Animal Behaviour, Jack Bradbury, a behavioral ecologist Smotherman and Bohn traced striking and now a professor emeritus at Corsimilarities between the tunes of the nell University, and zoologist Louise Brazilian free-tailed bats and those of Emmons of the Smithsonian InstituThree songsters. Top to bottom: The parti-colored bat (Vespertilio songbirds. The bat song is as complex tion reported recordings of greater murinus), the broad-eared bat (Nyctinomops laticaudatus), and the and structured—as “songlike”—as that sac-winged bats, Saccopteryx bilinheart-nosed bat (Cardioderma cor). of songbirds, they reported. Both are eata, from Trinidad. “I used a shothierarchically structured, composed of gun mic and reel-to-reel recording gear,” New Zealand’s Mystacina tuberculata, hun- multiple syllables and phrases; among the Bradbury recalls. “The bats would land on ker down in a cleft of a tree or similar grotto bats they include chirps, trills, and buzzes. their roosts at dawn and sing like birds, to belt out their tunes. Others, such as the Bat song even has syntax, or rules for and in a low enough register that I could European Vespertilio murinus, sing both constructing a tune. For instance, in the hear them.” from roosts and on the wing, erupting into songs of the free-tailed bat only chirp sylThe study of bat song didn’t take off until song at the end of autumn when females may lables can be included in chirp phrases, this century, however, when recording equip- be seeking a male to spend the winter with. and buzz syllables belong in buzz phrases. ment became more portable, making it easier Male Brazilian (also known as Mexican) free- Yet there is also room for flexibility, so that to work in the wild. By now, song has been tailed bats, Tadarida brasiliensis, the species each male’s song is unique—rather like a documented in 20 of the 1116 known species that Bohn and Smotherman have studied the jazz player riffing on a tune. “Their songs of bats, although scientists suspect that many most, sing year-round, but especially during aren’t just honk-honk-honk or eee-eeemore are talented songsters. Some, such as mating season. eee,” Bohn says. “They’re polysyllabic; they SCIENCE sciencemag.org

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have sequences, temporal structures, and a IT’S A QUESTION that many bat researchtimed rhythm.” ers raise. For more than 50 years, songbirds Perhaps most surprising, Bohn and her have been the animal model of choice for colleagues discovered that these bats can investigating the roots of human speech. also quickly vary the syntax of their songs That’s because of the many parallels— in response to social circumstances, again developmental, behavioral, neural, and as songbirds do. This type of audio-vocal genetic—between how human children plasticity is rare in mammals, aside from learn to speak and how young songbirds, humans. For instance, Brazilian free-tailed such as zebra finches, learn to sing, explains bats can instantly (in less than 100 milli- Richard Mooney, a neuroscientist who studseconds) switch from belting out a court- ies bird song at Duke University in Durham, ship song to singing a territorial tune, if North Carolina. another male echolocates nearby. “It means But songbirds are not mammals. “They they can adjust their output—their songs— don’t have a mammal’s neural architecbased on what they hear,” says Cynthia ture,” Smotherman says. “So working out Moss, a neuroethologist and bat echolocation expert at the University of Maryland, College Park. “It’s a very exciting discovery, as is all the work on bat acoustic communication, because it shows that bats have the same degree of vocal flexibility as songbirds, and it gets at bats’ social behaviors,” which are as yet not well understood. Bohn is full of unanswered questions about bats’ social life and songs. But after enumerating them she pauses, her blue eyes twinkling. “Actually, there’s an even bigger question. Why don’t we use bats to study the evolution of human speech?” Bat expert Kirsten Bohn with bat song recording gear at Uxmal. 1336

how bats use song and how bats’ brains produce song may give us a better idea of the changes and adaptations that had to occur for human speech to evolve.” Mice that sing ultrasonic tunes have been suggested as a model, but questions remain about their abilities, whereas “bats’ vocal production is fertile ground,” Mooney says. The bat researchers have already found that certain bats use songs in a slightly more complicated way than do some songbirds. Many songbirds use a single “dual-function” song to both attract mates and defend territories. But both greater sac-winged and Brazilian free-tailed bats have distinct songs for courtship and territorial defense. And male free-tailed bats sing even when it’s not the mating season, a time when they’re in an all-male roost with a million other guys. “They may be using their songs for other social purposes,” depending on the situation, Smotherman says. Bird song researchers are miles ahead, Smotherman concedes. They know the regions in a bird’s brain that produce song, and the selective pressures, such as female choice and male-male competition, that caused song to evolve. More than 100 labs worldwide, many with steady sciencemag.org SCIENCE

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PHOTOS: VIRGINIA MORELL/SCIENCE (2)

Scientists collect songs of Nyctinomops laticaudatus bats roosting in the walls of a ruin at Uxmal, Mexico.

PHOTOS: (TOP TO BOTTOM) KIRSTEN BOHN; MIRJAM KNÖRNSCHILD/ULM UNIVERSITY (3); KIRSTEN BOHN; STUART PARSONS; JON RUSS; GRACE SMARSH

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funding, explore bird song from all angles; other males in countersinging bouts. They push bats up to the level of birds in studies there are dedicated conferences and a sup- air these latter territorial tunes at dawn about the origin of speech. portive website, http://songbirdscience.com. and early in the evening when females are That’s why Bohn carted both recording Although bird song researchers would most likely to be away. The song lasts a mere and broadcasting equipment to the palace’s welcome a comparative mammalian model, 1.6 seconds, yet contains some 20 syllables wall at Uxmal. She and her graduate stuthe nascent study of bat song has nothing and ends with loud, low-frequency buzzes dent assistant Fernando Montiel run cables to compare with this. Bat song research- that are individually distinct and advertise from their laptops over the ancient stones to ers are still identifying which species sing the male’s strength. And there’s a big pay- a pair of microphones and a single speaker and in what social situations. “There’s such off for a song well sung: Male sac-winged on a long bar atop a tripod. Montiel raises variation in the songs and their functions,” bats that sing the most territorial songs at the array and points the speaker and microKnörnschild says. Some sound deceptively the lowest frequency father more offspring. phones at the wall’s fissures, where the small simple. The male Seba’s short-tailed bat Knörnschild is investigating the possibility bats lurk and sing. By now, my ears are tuned (Carollia perspicillata) from Central and that this species has culturally transmitted to their tiny melodies, and I, too, can tell the South America rhythmically repeats one dialects, as humans and some birds do. difference between an aggressive call and a variable note over and over, much like a Young sac-winged bats (and likely those rhythmic ditty. frog calling, Knörnschild says. Within that of other species) must learn these complex Earlier, Bohn and Montiel had recorded simple tune, however, there is an “individ- songs from their parents. Knörnschild and some of the bats’ songs, and, using specialual vocal signature,” a sound that identifies the caller and may help a female find her Singing for love and territory chosen mate, Knörnschild At least 20 bat species produce songs, which can be as flexible and complex as bird song and her colleagues reported in April in Behaviour. SPECIES LOCATION SONG TYPE SONG DESCRIPTION The crooning of other bats is more baroque. A team of Tadarida North and Courtship Rhythmic, multisyllabic brasiliensis South America trills, chirps, and buzzes researchers from the Czech Republic has decoded much Saccopteryx Central and Courtship Complicated multisyllabic of the courtship song of male bilineata South America phrases, with various trills European Pipistrellus nathuSaccopteryx Central and Territorial Low-frequency buzzes; males sii, a migratory species that bilineata South America with the most and lowest sings both on the wing and calls sire the most chicks from a roost. The scientists analyzed nearly 3000 recordCarollia Central and Courtship Repeated monosyllabic perspicillata South America trills ings they had gathered at 33 roosts in southern Bohemia, Nyctinomops Central and Possibly Multisyllabic with chirps, and reported in Acta Chiroplaticaudatus South America courtship trills, and buzzes terologica in 2008 that these Mystacina New Zealand Courtship; possibly Trills, sweeps, and tones, songs are semantically structuberculata lekking competition with ultrasonic components tured. The rhythmic tunes begin with a phrase (which Pipistrellus Europe Courtship at roost Multisyllabic phrases the scientists designated as nathusii and while flying and location information motif A) announcing the bat’s Cardioderma East Africa Territorial, but Low-frequency twitters and species, include an individual cor outside of roost trills that carry long distance vocal signature (motifs B and C), information about the bat’s population (motif D), and a signal about where to land (motif E). her colleagues found that male and ONLINE ized software, altered them so “Hence, translated into human words, the female sac-winged bat pups learn that they sound like the tunes of Listen to bat message ABCED could be approximately: songs by babbling and imitating, as songsters at different, unknown individuals. (A) ‘Pay attention: I am a P. nathusii, (B, C) do human infants and the chicks of http://scim.ag/ As soon as Bohn broadcasts the specifically male 17b, (E) land here, (D) we many bird species. (Although the 6190_media. remixed bat songs, the palace share a common social identity and com- females don’t sing as adults, they residents burst into twitters and mon communication pool,’ ” the research- need to know the songs in order to choose trills, which the scientists capture both in auers wrote in their paper. a mate.) Some bat species may even be able dio files and sonograms. These pulse across Even more complicated are the court- to imitate new songs throughout their lives, the screen of Bohn’s laptop like miniature ship songs of the greater sac-winged bats, Knörnschild, Bohn, and Smotherman think. lightning strikes as she watches transfixed. Knörnschild says. “When you look at their Only some songbirds possess such “vocal “We’re getting territorial buzzes, and sonograms, they are as complex as [those plasticity”; most songbird chicks have only some contact calls, I think. They know depicting] the melodies of nightingales. a short developmental period during which there’s an intruder. And, yes! That’s what I They have motifs within motifs.” A male sac- they’re able to learn songs. To clinch the want. One of the guys is trying to match the winged bat roosts during the day in a tree case for bats, these scientists say, someone intruder’s song.” That’s just the kind of hard hollow or grotto with a harem of females. needs to show an adult bat imitating another evidence for long-term vocal learning and He uses a song with soft tones to lure the adult bat’s song. “That would be the ultimate plasticity that she and Smotherman were ladies, and a harsher tune to compete with proof,” Smotherman says, and could help hoping for. ■ SCIENCE sciencemag.org

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When the bat sings.

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